After briefly rooming with Lesh in Las Vegas and returning to the San Francisco Bay Area, Constanten performed with an improvisational quintet formed by Steve Reich. The group's unusual style was influenced by both jazz and Stockhausen. In a 1964 performance, the ensemble played serialism-influenced compositions by both Constanten and Lesh. Although he walked out from the performance, minimalist composer Terry Riley later allowed the ensemble to premiere In C. However, only Reich and one other member of group, saxophonist-composer Jon Gibson, appeared in the seminal performance.[3]

Faced with the possibility of conscription amid the escalation of the Vietnam War, Constanten enlisted in the United States Air Force in 1965 as a computer programmer. Although the Air Force was deployed in southeast Asia, he was not given a security clearance after divulging his past communist sympathies and remained stationed domestically; while on leave, he used LSD and composed music on military IBMmainframe computers. By 1967, he had been promoted to E-4 and was stationed at Nellis Air Force Base near Las Vegas when he first collaborated with the Grateful Dead as a session musician on Anthem of the Sun (1968); Constanten used several compensatory three-day passes to travel to Los Angeles to record with the band. After sitting in with the band during live performances as his schedule permitted, the day after an honorable discharge, TC made his stage debut with the Dead as their permanent keyboardist on November 23, 1968 at the Memorial Auditorium in Athens, Ohio. He remained with the group for three albums and left after the band's infamous New Orleans drug bust following a January 30, 1970 show at the Warehouse. "It was like a magic carpet ride that was there for me to step on," he says. "I would have been a fool not to." Although Constanten nominally replaced founding keyboardist Ron "Pigpen" McKernan, the latter musician stayed on with the band as a frontman-percussionist; in light of their mutual abstinence from psychedelics, they became "as close as two heterosexual males could be", shared a house in Novato, California, and bunked together while touring.

While he had successfully contributed to their complex experimental music, his instrumental style was then grounded in classical technique and bore little consanguinity with the folk, blues, and country and western stylings that would largely anchor the band's oeuvre throughout the early 1970s. As well, there was some feeling that he did not fit in with the Dead ethos; for example, he was involved with Scientology throughout his tenure with the band and thus declined to become re-involved with LSD.[4][5] According to band manager Rock Scully, "He was sooo different. You know, he was like a crew cut. He was like a marine in a prison camp full of Japanese. He was like our boss in a way. Nobody could go for the hard wire technology of his brain power. I was told I was too hard on him, too. But I had no beef."[6]

From 1986 to 1993, he was the house pianist for the radio program West Coast Weekend, playing solo piano and interstitial music.[7]

I know of no path that is better marked than the study of music. Maybe I just think so because it's the path I'm on. There's the old question "How come there's never enough time to do it right, but there's always enough time to do it over." Well, here's an answer. Settle down. Do it right. However long it takes. That's the direct route to the fast lane!